This is the finale to my three-part blog series on the evolution and fossil record of Enhydra - I hope that you leave with 1) a sense of clarity about what we *do* know after all and 2) a sense of longing for finding out more - there is simply a lot that we don't know, even about the history of rocky shore faunas in general. It is my profound hope that someone interested in otter evolution will read this and get inspired to look into one of these new directions. This series will be updated in the future as more on our fossil otter research comes to fruition - our studies of the Gubik Enhydra and expanded hypodigm of E. macrodonta are just starting - so there are no preliminary insights from either project I feel comfortable with sharing yet. Go forth and discover some fossil otters!
The Thornton Beach otter - the oldest Pacific basin Enhydra
When I was a Ph.D. student in New Zealand I was nearly as far away as you can get on earth from these sea otter bearing localities, and had already grown so frustrated with my lack of results that I gave up trying. Earlier in my career I had tried looking for Plio-Pleistocene marine mammal fossils in the Merced Formation, much, much closer to home – the Merced Formation is exposed on the San Mateo Peninsula between Pacifica and Ocean Beach in San Francisco. However, localities of this unit require very long hikes up and down cliffs that are several hundred feet tall, and at least a couple of areas where I have not exactly felt safe. My first visit had crime scene tape at one – which I ignored – and upon returning home, my mother, who is a judge, recalled “oh yeah, there was a murder down there last week.” No thanks!
The rugged type section of the Merced Formation - a critical stratigraphic section for studying invertebrate biostratigraphy and climate across the Pliocene-Pleistocene transition. This is the view north from Mussel Rock; Fort Funston is at that far point, and north of there, Thornton Beach and Ocean beach. The Marin Headlands are the far hills in the distance across the Golden Gate (not visible). Photo from californiabeaches.com
Marine mammal fossils do occur in the Merced Formation, but they are extremely rare relative to the Purisima Formation further south that I was more used to: the Merced Formation was deposited about 5-10 times as rapidly, so the bones are dispersed and do not occur in easily accessed phosphatic bonebeds. I did about a half dozen trips between 2004 and 2006 and didn’t find a single bone. Needless to say, I knew intuitively that if I did not find any fossils, someone else might- but I might be an old man before that happened, since the last marine mammals were collected in the 60s!
The femur after preparation was perhaps halfway complete - thanks to RE Fordyce, and Sophie White for letting me prepare this in the Otago Geology Museum preparation lab!
Needless to say, I was pleased, excited, and a little in shock when I received some photos of a bone in a concretion in an email from my buddy Chris Pirrone – a civil attorney in the bay area who is an avid, ethical, and very generous fossil collector. Chris has also helped me with several excavations of whale and dolphin skulls! This specimen appeared to be a five inch long sea otter femur, but about 3/4 of it was still embedded and there is no shortage of land mammal bones from the upper parts of the Merced Fm. Nevertheless, from the little that was exposed I was confident and so I asked Chris if he wouldn’t mind donating the fossil to UCMP – and he generously offered to mail the specimen to me in New Zealand for preparation. I spent about two weeks mechanically preparing the specimen and, in the process, developed a neck ache that refused to go away for about 5 months (I could only afford very cheap pillows in New Zealand, which did not permit my neck to recover quickly).
The published illustration of the Merced Fm. otter, complete with ammonium chloride coating! From Boessenecker (2018).
The excellent stratigraphic control of the Thornton Beach sea otter - thanks to high resolution strontium dates from Ingram and Ingle (1998).
After preparation, the femur appeared to be longer than modern Enhydra lutris (reported also for a couple Enhydra sp. femora from the Pleistocene of Oregon), but still very clearly a specimen of Enhydra. After asking Chris details about the locality and stratum, it became clear that it was from a very well-dated horizon – where individual Strontium isotope dates were collected and reported every 5-10 meters (Ingram and Ingle, 1998), which is unusually high resolution for what I am used to! So I waited to publish anything (also, so I could finish my thesis on eomysticetids) until I was able to visit the locality myself with Chris and he could point to the individual rock layer. We visited the spot together in Summer 2015 after Sarah and I had returned from New Zealand, and I was able to pinpoint the stratigraphic interval to a horizon bracketed by dates of 620,000 to 670,000 years. After exhaustive reading of the stratigraphic literature, this was clearly the oldest known specimen of Enhydra from the Pacific basin.
Possible hypotheses for sea otter evolution & biogeography
There are two major hypotheses used in the evolution of sea otters from riverine ancestors.
Hypothesis 1) Enhydra evolved in North America, from something like Enhydritherium – the only other Enhydra-like otter from the north American fossil record.
Hypothesis 2) Enhydra evolved somewhere in the old world and had a more recent dispersal to the Pacific – either westward through the Central American seaway prior to Panama uplift about 3 Ma or through the arctic afterwards, or perhaps from east Asia along the north Pacific coast.
Unfortunately, most of the fossils are super fragmentary, as discussed in the prior blog post – virtually all specimens of Enhydra are isolated elements and not complete enough to code. There are also not a whole lot of characters available, and even when adding some to the Wang et al. 2017 matrix, I didn’t get much out of it. Nevertheless, the Wang et al. phylogeny does cast doubt on a close relationship between Enhydritherium and Enhydra – echoing the comparisons by Lambert (1997) with the more completely preserved skeleton of Enhydritherium from Florida. While we don’t have a reliable phylogeny, we DO have some pretty reliable characters to identify these things – Enhydra teeth are very distinctive, and we do have geochronology. This information cannot answer problems of phylogeny (e.g. which forms of extinct Enhydra are more closely related) but it most certainly can tell us where Enhydra was and when.
The two different results of the phylogeny of lutrines (otters) by Wang et al. (2017); the one on the left is better resolved (50% majority rules consensus tree), and shows a close relationship between Enhydra and Enhydriodon, which is not resolved in the second phylogeny under Bayesian methods; however, a close relationship between Enhydra and Enhydritherium is unlikely owing to the well-resolved sister taxon relationship between Paludolutra and Enhydritherium.
Revision of the biochronology of sea otters in the North Pacific
Hypothesis 1 listed above, endorsed by Mitchell (1966) and Repenning (1976), has two requirements: firstly, that fossils of Enhydra truly pre-date Enhydra reevei from the UK, and secondly, that there is a close relationship between Enhydra lutris and Enhydritherium. Phylogenetic analysis by Wang et al. (2017) calls the latter into question. So what about the dates? My review of up-to-date stratigraphic research found that all Pacific basin specimens of Enhydra are from the late or middle Pleistocene. In particular, the Timms Point Silt tooth which was so critical to Mitchell’s dismissal of Enhydra reevei – is no older than 400,000-500,000 years in age. The Timms Point Silt specimen is therefore at least 1-1.5 million years younger than the British specimens, and 100,000-200,000 years younger than Chris Pirrone’s femur from San Francisco. The significance here is that updated geochronology tells us that once again, Enhydra reevei is the oldest bone fide example of a fossil Enhydra anywhere in the world. This on its own, along with the re-shuffling of Pacific coast specimen ages, knocks out one of the two requirements for the Mitchell hypothesis and is suggestive of a relatively recent invasion of the Pacific basin. One caveat is that while late Pliocene strata like the San Diego Formation are very well-sampled, there are virtually zero early Pleistocene marine mammal bearing localities where more than ten individual specimens have been discovered anywhere in the eastern Pacific. As for the second requirement, a close relationship between Enhydra and Enhydritherium does not seem to be likely, thanks to the Wang et al. (2017) phylogeny.
Revised biochronology of Enhydra fossils. All of them. From Boessenecker (2018).
What about those fossils from Alaska? At least one or two specimens from the Gubik Formation indicate the presence of Enhydra in the Arctic about 1.5-2 million years ago, slightly younger than the British fossils. Because of these, and the fact that the Central American Seaway would have already been closed after 3 Ma, I proposed in my 2018 paper that Enhydra evolved from Enhydriodon in western Europe during the Pliocene and dispersed through the Arctic, into the North Pacific, during the early Pleistocene. An earlier dispersal is not tenable at present owing to the well-sampled San Diego Formation, and derivation from Enhydritherium seems unlikely.
This is quite surprising as it means that the modern kelp forest ecosystem, seemingly dependent on sea otters to keep urchin numbers down, was very different only one million years ago. Who used to eat all the urchins? I honestly have no idea – walruses don’t really eat urchins, to my knowledge, and they’re some of the only durophagous predators from the Pliocene.
In conclusion: the oldest bona fide Pacific basin fossils of Enhydra are less than one million years old, and since older fossils exist in the Atlantic, sea otters probably evolved in the late Pliocene in western Europe and immigrated to the North Pacific very recently.
Why are sea otter fossils so rare? Even during their established geochronologic range, otter fossils are quite rare. To be honest, all marine mammals are rare in Pleistocene deposits – but it’s much easier to find pinniped fossils, for some reason. One argument is that otters tend to be restricted to rocky shore environments – which are environments characterized by erosion rather than deposition, so they’re already biased. Sea otters are quite small – and small vertebrates have a lower preservation potential than larger vertebrates, right? For example, there’s the ‘colloquial knowledge’ about how rare it is to come across a bird carcass that isn’t just a pile of feathers. Could taphonomy explain the rarity of sea otters? Carcass drifting experiments using… car tires, in the 1990s, showed that they modeled the drifting behavior of sea otters quite well. Sea otters tend to float if they die at the surface, owing to large lungs. Sea otter carcasses typically float for up to six weeks – which, surprisingly, is just as long, if not slightly longer, than harbor seals and dolphins observed by Willhelm Schafer in the North Sea. What does this extreme floating v. body mass ratio mean? Probably several things:
1) Because sea otters don’t exhale when they dive, and do not dive deep, this could make the discovery of complete skeletons very rare, as most end up on shore rather than sinking.
2) Because sea otters live so close to shore, most carcasses are probably going to end up drifting towards the shore at some point. Indeed, carcass and dummy drift experiments have 2/3 of each washing up on shore. The shoreline environment is one of the highest energy marine environments, and preservation of marine vertebrates in any meaningful volume is rare: only a handful of vertebrate fossil sites have ever been demonstrated to really represent this environment, and most rich assemblages of marine mammals represent deposition in at least 10 meters water depth. Virtually all stranded carcasses will not enter the fossil record except as unrecognizable bone pebbles and pulverized sand-size particles. It is for this reason I am utterly skeptical of the utility of many studies of taphonomic patterns of stranded carcasses. Stranded carcasses also give us meaningless data on disarticulation, because continually floating carcasses never undergo drying of the tissues, but that’s another problem.
Sea otter carcass and car tire drift experiments - Young et al. 2019.
3) Floating carcasses have the opportunity to shed isolated elements, particularly from the extremities, as they disarticulate – if they have enough time to decompose enough.
4) The distance of transport and the likelihood of stranding depends entirely upon currents and wind direction, which varies seasonally and daily. This is likely why 1/3 of the carcasses from the experiment never stranded, and why some drifted 100-200 km, which is still quite far. This drift distance casts doubt on ever being able to infer habitat preference from the fossils, as one carcass can, in its post-mortem road trip, cross virtually ever environmental boundary on the steep, narrow California shelf. Any discoveries of sea otter bones and teeth in rocky shore environments may be completely accidental.
5) Lastly, I’m not sure if comparable carcass drift experiments with larger seals and sea lions exist – but I expect them to differ little. The larger a marine mammal is, the higher the capacity for long-distance carcass transport. Sea otter drift patterns mean that it’s possible for partial skeletons to sink after the ‘bag of bones’ stage of bloat and float down into middle shelf sediments, where they are less likely to be scoured and separated by bottom currents. So why are most of our sea otter fossils from shallow settings adjacent to rocky shore environments?
Rocky shore environments, like the Monterey headlands, are characterized by erosion rather than deposition - which heavily biases the rock record and fossil record against rocky shore faunas, and since most marine mammals from the eastern North Pacific are found in these scattered deposits - their remains are often quite poorly preserved. Photo by RWB - the famous Lone Cypress on 17 mile drive in Pebble Beach, CA.
There are precious few pre-Pleistocene rocky shore faunas on the west coast: this is because rocky shore fossil assemblages are deposited as geographically limited lenses around sea stacks or other rocky exposures. These rocky exposures indicate the long-term likelihood of erosional destruction. Therefore, most rocky shore faunas from California, for example, probably have a short shelf life of 1-2 million years. True marine deposits formed by basin subsidence, rather than resistant bathtub rings around bedrock, are frequently thicker and more laterally extensive – but also generally terminate about 2 million years ago, when the California coast ranges began to be uplifted and all of the large shallow marine embayments dried up (now the SF Bay area, the Salinas river valley, the LA basin, and others). Two notable exceptions are the Port Orford Formation of Oregon, which is middle Pleistocene, and the upper part of the Merced Formation near San Francisco, which is middle Pleistocene in age (lower Merced is late Pliocene). It is possible that fossils of Enhydra will be found in Pliocene shelf deposits in California or Japan – after all, we assumed the same thing about monachine seals, until my good friends Jorge Velez-Juarbe and Anita “Phocita” Valenzuela-Toro (2019) reported a couple of monachine seal teeth from the Monterey Formation of Orange County, CA. So, it’s possible – but the evidence just isn’t there yet.
So what makes fossil sea otters rare, in my opinion? I’m not sure genuine scarcity has anything to do with it, and I am always hesitant to ascribe any paleoecological reasons, as dead animals float around all over the place and cross these convenient ecological boundaries rapidly after expiring (and, relative to body mass, sea otters take this to an extreme). Do sea otters have high preservation potential? Certainly it’s not much lower than that of pinnipeds, as their bones are still large, but smaller and perhaps slightly more easily abraded than seal and sea lion bones. We also have no shortage of tiny pinniped and dolphin skeletons in the rock record. Their preservation potential has to be much higher than sea birds – however, sea birds actually have a surprisingly high preservation potential, and are remarkably common fossils in Neogene marine deposits (even at places like Moonstone Beach – bird bones outnumber marine mammal bones by 10:1). So, maybe sea otters are rare – but there’s so much in terms of unknown variables I will hesitate for a long time before ever suggesting that as a viable hypothesis. In sum, I do not think there is enough that is fundamentally different in terms of anatomy or ecology, either from numerically common sea birds or small fur seals, that might explain the rarity of fossil sea otters.
Rather, I think it is an artifact of rock bias: there is a fundamental disconnect between the rich open shelf deposits of the Miocene/Pliocene and the rocky shore bathtub rings of the Pleistocene: the Pleistocene deposits are small in volume, geographically disparate, with poor (and rapidly shrinking) exposures. They are also generally terrace deposits that do not benefit from the typical sedimentological processes that concentrate vertebrate fossils in open shelf environments. Because 1) there is this difference in the abundance of marine mammal fossils between Pliocene and Pleistocene deposits owing to sedimentological factors, 2) difference in the volume of rock and area of exposure between these two epochs, and 3) sea otters are Pleistocene-only in the Pacific, sea otter fossils are rare. If we had open shelf deposits with preservation/sedimentology more similar to Neogene deposits like the Purisima and San Diego Formation, there would probably be more fossils of Enhydra on the west coast.* In conclusion, while rock bias cannot on its own explain the lack of pre-Pleistocene sea otters (bloat and float would have introduced at least a few sea otters into units like the San Diego Formation), sea otters invaded at a time when virtually all relevant deposits are scattered and limited in volume. So there are scraps instead of skeletons (unlike the Pliocene record of marine carnivores).
*”But what about Enhydritherium?” I hear someone moaning somewhere in the distance. Enhydritherium is Pliocene and therefore should be found in Pliocene marine deposits more frequently. Do recall that this species is probably not open marine and is probably freshwater-estuarine in distribution and therefore is not a good analog.
When did tool use evolve? We don’t really know, since there aren’t really many skeletal adaptations other than tiny forelimb size that correspond to tool use. The modern clawless otters are very dexterous, but do not use tools, and have river otter like limb proportions – suggesting that the bizarrely tiny forelimbs of Enhydra are a reasonable skeletal correlate. Enhydritherium is one of the only proposed Enhydra relatives with good postcrania, but it has river otter-like fore/hindlimb proportions. We don’t have much in the way of postcrania of Enhydriodon that is informative. There are isolated humeri from southern California of middle and late Pleistocene age that are anatomically identical to modern Enhydra lutris, and which Mitchell (1966) referred to the extant species. This would at minimum suggest – if the humeri are identical in size (difficult to evaluate owing to the fact that these are isolated elements) – that tiny forelimbs have been present in the sea otter lineage for a few hundred thousand years.
Who filled the otter niche before the Pleistocene? The modern kelp forest ecosystem probably originated in the late Miocene (Estes and Steinberg, 1988) - and today, sea otters are a keystone species: without otters, sea urchin populations get out of control and raze most of the kelp forest to the ocean floor. These "urchin barrens" now dominate rocky coasts between Monterey and British Columbia. The purple urchin, Strongylocentrotus purpuratus, is one of the most distinctive west coast marine invertebrates, and has a voracious appetite for kelp. This species is known from the Pliocene San Diego Formation, and certainly pre-dates Enhydra. So who ate urchins and kept their populations down before the arrival of sea otters? Sheepshead wrasses (Semicossyphus pulchrer) eat them - and have a fossil record in California extending *probably* back to the late Miocene owing to abundant tooth plates found in the Santa Margarita Sandstone. Annarichthys - the horrifying but very gentle and shy wolf eel - feeds on urchins, and is known from the Purisima Formation. Some sea stars (with admittedly a very limited fossil record on the west coast) feed on them. Would some of the extinct walruses have filled the niche of sea otters? Modern walrus occasionally feed on urchins, but they are probably second rate food consumed when more favorable mollusks are not available (Sheffield, 1997). My money is on durophagous fish - but more research is clearly needed on the evolution of rocky the shore fauna and flora!
*This species has extra relevance to my family. My mom told us of her first field trip as a grade school student (St. Gregory's in San Mateo) to the Fitzgerald Marine Preserve in Moss Beach CA - indeed my first tidepool I ever visited - which was cancelled about 10 minutes after arrival because class idiot "Patrick R" stuck his tongue into a purple urchin and it became so swollen he couldn't breathe. Patrick had earlier gotten his head stuck in a chair during class.
Otter tool use leaves distinctive patterns of breakage on mussel shells - from Haslam et al. 2019.
Will we ever find sea otter tools in the fossil record? My guess is, probably not. There's one paper out there documenting what sea otter anvil stones and accumulations around them look like - but the odds of finding one in a rocky shore deposit are staggeringly tiny in my opinion. What is far more likely is looking at the distinctive patterns of breakage of different species of mollusks, like Haslam et al. (2019) did, and looking for those same patterns of breakage in the fossil record. This might even turn up more of a record than actual sea otter bones, since there are many more Pleistocene rocky shore deposits that completely lack vertebrates than there are that preserve them. As for the rocks that sea otters bring along with them? As discussed in part 1, it's not clear that the whole "sea otters carry around their favorite rock!" claim is more than a popular factoid, and doesn't seem to have a basis in scientific observation. We don't know how long sea otters carry their hammer stones around, or if the banging leaves any observable traces on them; indeed, it's not even clear if the anvil stones would be recognizable either without observation of otters using them. So, I don't think we'll be able to have a sea otter technology 'parataxonomy' like the "Oldowan" technology in the east African rift valley for early humans just quite yet.
When exactly did otters arrive in the Pacific? The lack of well-sampled early Pleistocene deposits in the eastern North Pacific precludes a precise estimation. We know it was sometime before 600,000-700,000 years ago, unless the Thornton Beach sea otter is the very first individual. However, we’re pretty certain that it was after the Plio-Pleistocene boundary 2.5 million years ago, since no sea otters (Enhydra spp) have ever been found in densely sampled units like the Purisima and San Diego formations. I predict that by the time I retire, zero fossils of Enhydra will be discovered in Pliocene rocks of the Pacific coast, and will happily eat my hat if this prediction turns out to be wrong.
Which lineage of freshwater otters did Enhydra evolve from? This is going to require more skulls of Enhydriodon and a significantly expanded morphological matrix for otters, in concert with molecular data in a combined analysis. I’m not interested in doing this, as to be honest, I really only care about sea otters and aside from them being adorable, don’t really give two shits about the phylogeny of river otters. But, someone will have to: right now our only ‘good’ phylogeny has about two dozen species and only 40ish morphological characters, with lots of uncertainty (Wang et al., 2017). The Wang et al. matrix is a fantastic start, don’t get me wrong – and it does hint at Enhydriodon-affinities of Enhydra, and casts doubt on an origin from Enhydritherium in North America.
1) We really need more fossil otters. Future exploration of latest Pliocene and Pleistocene (early, middle, and late) units, especially near Los Angeles, the Channel Islands, the Merced Formation near San Francisco, the Humboldt County localities, southwestern Oregon, and the Gubik Formation of Alaska will produce more otter material. More fossils will help with further clarifying the geochronologic range of Enhydra, and hopefully add to the hypodigm of Enhydra macrodonta, and perhaps reveal the existence of other species in the Plio-Pleistocene transition. We also need to be creative and reach out more to amateur collectors in northern California and Oregon who may have already collected some fossil otter material; thus far I’ve been pretty secretive about my otter research for various reasons, but I think getting the word out about how little we know about fossil sea otters, and what we *think* is going on, is a better course of action. We also need to go out and explore more Pleistocene marine mammal localities; the San Pedro Sand and Palos Verdes Sand near LA have been explored *somewhat* but there is undoubtedly more that can be done, provided there are surviving outcrops. We’re down to one major locality left (Moonstone Beach) in Humboldt County since Crannell Junction was overgrown in the 1980s, and it’s smaller than it used to be. Another option further south needing more field exploration is the Santa Barbara Formation – which is very well-exposed near Coal Oil Point in Isla Vista, a site I haven’t visited since I was in High School. There are some marine mammal scraps from that locality, and I think seasonal visits by some of my colleagues in Southern California could turn up some precious Pleistocene marine mammal material.
2) A reevaluation of Enhydra macrodonta is needed, including description of referable specimens from the same locality. This is a planned study with Ash Poust for the near future.
3) An interesting partial skull of Enhydra (identified in 1983 by Repenning as E. lutris), from the Gubik Pliocene-Pleistocene Formation of Alaska, awaits description – and is currently under study by yours truly, with assistance from Ash Poust, Morgan Churchill, and invertebrate paleontologist Chuck Powell. I won’t spoil it, but some aspects of it are pretty exciting (for example, sea otters cannot inhabit the Arctic ocean today because of the sea ice).
4) A more exhaustive phylogenetic analysis of lutrines is desirable, but this may be too much of an ask.
5) Granting agencies really need to be more supportive of field-based paleontology that doesn’t involve looking for dinosaurs in places we’ve found them for over 100 years.
Boessenecker, 2018. https://link.springer.com/article/10.1007/s10914-016-9373-6
Estes and Steinberg, 1988. https://www.jstor.org/stable/2400895?seq=1#metadata_info_tab_contents
Haslam et al. 2019. https://www.nature.com/articles/s41598-019-39902-y
Ingram and Ingle, 1998. https://www.sciencedirect.com/science/article/abs/pii/S0033589498919901
Lambert, 1997. https://www.jstor.org/stable/4523861
Repenning, 1976. Repenning, 1976. C. A. Repenning. 1976. Enhydra and Enhydriodon from the Pacific Coast of North America. Journal of Research of the United States Geological Survey 4(3):305-315.
Sheffield, 1997. http://www.adfg.alaska.gov/static/home/library/pdfs/wildlife/research_pdfs/walrus_feeding_re_examination.pdf
Wang et al. 2017. https://www.tandfonline.com/doi/abs/10.1080/14772019.2016.1267666?journalCode=tjsp20
Young et al. 2019. https://onlinelibrary.wiley.com/doi/abs/10.1111/mms.12609